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The Journal of Neuroscience, January 11, 2006, 26(2):479-489; doi:10.1523/JNEUROSCI.3915-05.2006

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Cellular/Molecular
Electrical Hyperexcitation of Lateral Ventral Pacemaker Neurons Desynchronizes Downstream Circadian Oscillators in the Fly Circadian Circuit and Induces Multiple Behavioral Periods

Michael N. Nitabach,^1,2 Ying Wu,² Vasu Sheeba,¹ William C. Lemon,³ John Strumbos,² Paul K. Zelensky,³ Benjamin H. White,³ and Todd C. Holmes¹

¹Department of Biology, New York University, New York, New York 10003, ²Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06510, and ³Unit on Neural Function, Laboratory of Molecular Biology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892

Coupling of autonomous cellular oscillators is an essential aspect of circadian clock function but little is known about its circuit requirements. Functional ablation of the pigment-dispersing factor-expressing lateral ventral subset (LN_V) of Drosophila clock neurons abolishes circadian rhythms of locomotor activity. The hypothesis that LN_Vs synchronize oscillations in downstream clock neurons was tested by rendering the LN_Vs hyperexcitable via transgenic expression of a low activation threshold voltage-gated sodium channel. When the LN_Vs are made hyperexcitable, free-running behavioral rhythms decompose into multiple independent superimposed oscillations and the clock protein oscillations in the dorsal neuron 1 and 2 subgroups of clock neurons are phase-shifted. Thus, regulated electrical activity of the LN_Vs synchronize multiple oscillators in the fly circadian pacemaker circuit.

Key words: arrhythmia; behavior; circadian rhythms; desynchronization; Drosophila; sodium channel

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Received Sep 15, 2005; revised October 25, 2005; accepted November 15, 2005.

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